The greatest focus when it comes to sports concussion
has been in the attempt to develop diagnostic
testing to evaluate athletes who are suspected
of having suffered a concussion. Testing
ranges from simple sideline evaluation tools to complex
neuroimaging studies. None of the diagnostic
studies are completely objective and should never be
used as the sole means of assessment or in deciding
when to return an athlete to play. The best way to
assess an athlete or any individual who has sustained
a concussion is still a comprehensive neurological
history and detailed neurological examination
performed by a properly trained physician.

Definition of Sports Concussion

A prolonged transient alteration in neuronal function caused by a
blow to the athlete's head and/or body with transmission of force
to the head, resulting in rotational and/or translational (i.e.,
angular and lateral) movement of the head resulting in
neurological symptoms that resolve sequentially over time.

Sideline Concussion Assessment Tool (SCAT2)

Developed in 2008 to replace the original sideline
assessment tool SCAT1, SCAT2 is intended to assess
individuals aged 10 and older and can be used by
almost anyone after a brief training session.1 It is
used by a number of professional and amateur
sports organizations and is usually given at the start
of the season and repeated if an athlete sustains a
concussion. The test has many of the same components
of the standard neurological exam, with eight
subsections including; symptoms, physical signs,
Glascow coma score, Maddock's score, cognitive
assessment, balance assessment, coordination and a
standardized concussion assessment (Glascow coma
score and Maddock's score do not apply if using the
test as a baseline assessment). Many concussion
experts do not use the Glascow coma scale because
loss of consciousness is present in less than 10 percent
of all athletes. Portions of the test have not
been validated and therefore SCAT2 should never be
used as the sole measure to return an athlete to play,
or as a substitute for a physician-performed neurological
evaluation.

Computerized Testing

Most professional, college, and some high school
sports teams use computerized testing IMPACT,
Headminder Concussion Resolution Index (CRI)
(New York, NY), CogSport (CogState, Melbourne,
Australia), and the Automated Neuropsychological
Assessment Metric (ANAM) [Center for the Study
of Human Operator Performance, The University
of Oklahoma, Norman]. Athletes are tested by a
trainer or neuropsychologist prior to the start of
the season and during the season if a concussion is
reported. These tests are useful tools for evaluating athletes, and despite being validated with formal
neuropsychological testing, they should never be
used as the sole means for returning an athlete to
play and should never be substituted for a comprehensive
history and neurological examination.

The most widely used computerized test is
IMPACT, however most tests measure multiple
aspects of cognitive functioning, including:
Attention span, working memory, sustained and
selective attention, response variability, non-verbal
problem solving. Issues with computerized testing
include: Lack of initial effort (i.e., pre-season)
whereby the athlete will actually score better after
sustaining a concussion;2 An inability to address
associated symptoms (i.e., headache, sleep disorders);
3 Reaction time testing is marginal and does
not simulate game conditions. The tests are also
influenced by symptoms, such as headache and
lack of sleep, which are very common with concussion.
4-7

Furthermore, the tests do not appear to accurately
reflect the metabolic recovery of the injured
brain, as most high school and collegiate athletes
displayed functional/cognitive recovery at approximately
six days following a sports-related concussion,
while the professional athletes displayed
recovery within three days.8 This is inconsistent
with physiological recovery, which takes between
14-28 days.9 Finally, as the tests are often administered
on consecutive days, improvements in concussed
athletes may be partially associated with
learning effects and not with injury recovery.10-13

Neuropsychological Testing

Formal paper and pencil neuropsychological testing
is the best method to evaluate cognition in athletes
who have sustained concussion. The tests have
been validated in studies with non-athletes,14,15 but,
surprisingly, there are very few studies in concussed
athletes.16-18 Due to cost, length of testing,
and access, neuropsychological testing is mainly
used in athletes with prolonged cognitive symptoms.
Testing tends to focus on assessment of sustained
and divided attention, reaction time, visual
and auditory processing speed, and working memory.
Intelligence, problem solving and language are
also tested.16-18

Balance, Agility and Reaction Time Testing

After concussion, communication between sensory
systems is lost in the majority of individuals, causing
moderate to severe postural instability in either the
anterior-posterior direction, medial-lateral direction,
or both.19-21 Concussed athletes have demonstrated
balance deficits using both high-tech and clinical
methods of assessment.22-24 Decreases in postural stability
persist for up to three days following injury,
after which time the athletes gradually recover to
approximately the scores of matched control subjects
by day 10 post-injury.19,23 Vestibular deficits are
related to problems with sensory integration, whereby
the concussed athlete fails to use their visual and
vestibular systems effectively. Studies have demonstrated
difficulties with task switching in concussed
athletes.21 A number of tests are currently available
or in development including Balance Error Scoring
system (BESS), Sensory Organization Testing (SOT),
Gait Testing, Virtual Reality Testing, and
Instrumented Agility Task Testing.23,25 In addition,
there are components of the neurological exam
including Rhomberg (i.e. sway), finger-nose-finger,
fine finger testing, rapid alternating movement testing,
and tandem gait alone or in conjunction, that
may be useful in evaluating concussed athletes but
still need to be validated. The Balance Error Scoring
System (BESS) uses three different stances (double,
single, and tandem) which are completed twice—
once while on a firm surface and once while on
piece of medium-density foam.23 Studies have
revealed greater differences between injured and
uninjured subjects when the balance tasks became more challenging, such as by adding a foam surface
and narrowing the base of support.22 The test is also
part of SCAT2, and the only part of BESS to be validated
is the single leg stance portion.26 BESS is most
sensitive at time of injury up to three to five days
post-concussion.23

Concussed athletes have also demonstrated balance
deficits using a sensory organization testing
(sophisticated force plate systems).27 These tests provide
a more technical or refined measure of balance
performance by challenging and altering information
sent to the various sensory systems. Testing is limited
to use off the field and in academic centers secondary
to size and technology needs.

Others have attempted to assess athletes using
high-tech virtual reality testing.28 Finally, researchers
at the University of Michigan are in the process of
testing a “puck drop test” where a long stick weighted
with a hockey puck is dropped and the athlete
tries to catch it as quickly as possible. Marks on the
stick measure how quickly the athlete was able to
react. Seven of eight Division I athletes who had suffered
a concussion showed significantly slowed reaction
times with the device, which is currently undergoing
further testing.29

Eye Movement Testing

Galetta et al. have developed the King-Devick test
(K-D) to assess eye movement abnormalities in concussed
athletes.30,31 The test involves reading aloud a
series of single digit numbers on three test cards
from left to right. The sum of the three test card
time scores and the number of errors are scored.
The test is hypothesized to measure impairment of
eye movements, attention, and language. They
administered the test to a cohort of boxers (n=27)
and MMA fighters (n=12) pre- and post-fight. Postfight
K-D time scores were significantly higher
(worse) for participants who had head trauma (59 vs.
41 seconds), and those with LOC had higher post
fight K-D scores than those without LOC (65.5 vs.
52.7 seconds). Abnormal post-fight scores also correlated
with abnormal MACE scores. The authors suggested
that the test could serve as a rapid sideline
screening test.31 The study has not been validated in
other populations, i.e. ice hockey, football etc., and
there are issues with the timing of the post-testing,
including the time immediately after the fight, when
the athlete is physically fatigued and dehydrated.
Fatigue and dehydration are well known to effect
cognitive function and cognitive testing.32 In addition,
giving the test immediately after the fight
when the athlete's motivation may not be as high as
pre-fight and there are significant external distractions
can affect outcome.

The ID Coaches Sideline tracker is another test
that can measure eye movement abnormalities in
concussed athletes. The test looks for gaze abnormalities
and is given after an athlete is suspected of
being concussed. Blurred/double vision or inability
to focus may be indicative of concussion.

Electrophysiological Testing

McCrea et al.33 used Quantitative EEG Q-EEG in a
prospective, non-randomized study of 396 high
school and college football players, which included a
cohort of 28 concussed athletes and 28 matched controls.
All underwent preseason baseline testing
including postural stability testing, cognitive testing
and Q-EEG. Clinical testing was repeated on the day
of injury. They found injured athletes performed
poorer on neuro-cognitive testing than controls on
the day of injury but not at days eight or 45.
However, concussed athletes had abnormal electrical
activity noted on the day of injury and day eight,
but not day 45. They concluded that the duration of
physiological recovery may last longer than observed
clinical recovery. Dupuis et al. 2000 looked at eventrelated
potentials (ERP) to assess cerebral activity in
20 college athletes with MTBI. They found that concussed
athletes had a decrease in the P300 amplitude
and concluded that this may reflect alterations
in attention and concentration.

Biomarkers

The biotechnology industry and military are currently
looking at a number of biomarkers to measure
mTBI, both on the battle ground and in the clinic.

Apolipoprotein E (APOE), APOE promotor gene,
Catechol-o-methyltransferase (COMT), Dopamine D2 receptor (DRD2) (ANNK1 gene), Interleukin p53,
Angiotensin converting enzyme (ACE), CACNA1A,
SB100, have been or are currently being evaluated.
The two most widely studied are Apolipoprotein and
SB-100 with the later showing minimal efficacy in
detecting concussion in sports.34-37

Apolipoprotein has been looked at in a number of
studies in both athletes and non-athletes and has
been correlated as a marker for chronic injury. Zhou
et al.38 performed a meta-analysis and looked at 14
cohort studies. There was no correlation of the Â4
allele with initial injury severity. However, the Â4
allele was associated with poorer outcome at six
months after injury. Terrell et al. looked at 195 college
athletes, mainly football and soccer players. The
cross-sectional study investigated the association
between APOE, APOE promoter, and tau polymorphisms
and a self-reported history of concussion
over a prior eight-year period. There was a threefold
increase in risk of concussion in those with the
TT genotype of G-219T polymorphism relative to the
GG genotype, and a four-fold increased risk in those
a with self-reported history of concussion associated
with loss of consciousness. There was, however, no
association with APOE or tau genotypes.

Kristman, et al.39 in a prospective cohort study of
318 collegiate athletes in various sports, compared
concussion rates in athletes with and without APOE
Â4 allele. They found no association between Â4
allele and sustaining a concussion Finally, Tierney et
al.40 looked at 196 college athletes (163 male football
and 33 female soccer players) in a multi-center
cross-sectional study evaluating the association of
carrying 1 or more APOE rare (or minor) alleles
(APOE Â2, APOE Â4 and T allele of G-219T APOE
promoter polymorphism) and a self-reported history
of concussion. Athletes carrying all three rare alleles
were 9.8 times more likely to report a previous concussion.
Athletes carrying the T allele of the APOE
promoter gene were 8.4 more likely to report multiple
concussions and the authors concluded that carriers
may be at greater risk for multiple concussions.

Neuroimaging

Athletes who sustain concussion do not require routine
imaging. Exceptions include those with loss of
consciousness, increasing lethargy, and focal neurological
findings on their neurological exam. If the
athlete requires imaging, CT and conventional MRI
are both useful in detecting intracranial and subdural
bleeds, however they are usually without findings.
Conventional MRI with gradient echo is also useful
in detecting micro-bleeds and Diffuse Axonal Injury
(DAI) in more severely injured patients. More
advanced imaging such as Positron Emission
Tomography (PET), Functional MRI (fMRI),
Magnetic Resonance Spectroscopy (MRS), and
Diffusion Tensor Imaging (DTI) hold the most promise
for quantitative assessment of sports related concussion.
Ideally, imaging needs to provide quick,
reliable, and longitudinal capabilities, and be easily
employed in the community setting.

Positron Emission Tomography (PET) scanning
measures brain metabolism by using radio
nucleotides with short half-lifes. It is useful in measuring
quantitative brain glucose uptake and regional
oxygenation and therefore can demonstrate metabolic
disturbances after brain injury.41 There is little
data on athletes who have sustained concussion. One study looked at 19 boxers and eight normal controls.
The study demonstrated hypometabolic areas,
i.e., decreased glucose uptake in the bilateral posterior
parietal lobes that extended to the lateral occipital
lobes, bilateral frontal lobes, bilateral cerebellar
hemispheres, and posterior cingulate cortex.42 There
are also a few studies in patients with mTBI that
demonstrated correlation between metabolic dysfunction
and neuropsychological performance.43-45
Potential disadvantages include study duration, arterial
sampling for quantitative studies, lack of available
units in the community, the need to produce
isotopes on site/locally. The most important disadvantage
is that in patients with mild traumatic brain
injury, PET imaging studies appear to remain abnormal
after the recovery phase. The potential in sports
related concussion assessment is in the academic
setting to study brain physiology and metabolic
derangements associated with sports concussion.

Magnetic Resonance Spectroscopy (MRS) uses
metabolite data from regions of the brain to provide
an assessment of neuro-chemical alterations after
brain injury. Metabolites typically include N-acetylaspartate
NAA (neuronal specific metabolite and a
marker for neuronal health), myoinositol (glial marker),
choline (marker of inflammation), lactate (indirect
marker for ischemia and hypoxia), creatinine
and phosphocreatinine (stable brain metabolite and
marker of cellular energy status).46 Vagnozzi et al.47
looked at athletes with sports related concussion and
found a diminished NAA/creatinine ratio 12 days
after the athletes reported symptomatic recovery.
The major drawback with MRS is its relative availability
in the community due to scanner requirements
and software costs.

Functional MRI (fMRI) measures changes in
regional blood oxygenation that are usually quantified
based on Blood Oxygen Level Dependent activity
(BOLD). Following injury, decreases in blood flow
are therefore speculated to represent impaired functional
capacity.46 The study usually requires a patient
to perform a task while being imaged. Limited studies
using fMRI in sports related concussion (Lovell
et al.) have demonstrated abnormal BOLD activity,
which correlated with symptom scores and neuropsychological
testing. The studies also demonstrated
improvement in BOLD activity in patients whose
symptoms had resolved, implicating fMRI as a tool
to possibly assess recovery from concussion.

In addition, athletes who displayed hyperactivation
on a cognitive task in the acute phase had prolonged
recovery times relative to those athletes who
demonstrated typical activation in the acute phase
implicating fMRI could be used to predict who will
recover quicker.48 Functional MRI has also been used
in defining areas of the brain affected in sports concussion.
Jantzen et al.49 found increased activation in
the areas of the parietal, lateral frontal, and cerebellar
regions. Major limitations are software cost and
the duration of the test. Therefore, its use will be
limited to academic institutions and professional
sports teams.

Near Infrared Spectroscopy is a non-invasive technique
that evaluates cerebral blood volume and oxygenation.
The technology is based on the transmission
and absorption of near-infrared light as it passes
through tissue. Cote, et al. monitored cerebral hemodynamics
during acute exercise following concussion
in 14 male university hockey players and found
cerebral oxygenation was reduced up to 35 percent
on day one following concussion. Blood volume
increased immediately following a concussion at rest
and during exercise at day one and returned to baseline
by day seven. The authors concluded that there
is an increased demand for oxygenated blood following
concussion. This technology uses a hand held
scanner and has the potential to be used in office as
a screening technique.

Diffusion tensor magnetic resonance imaging
(DTI/MRI) uses state of the art high Field MRI (1.5T
and 3.0T) to evaluate the speed and direction of
water movement within axons, which is termed fractional
anisotropy or FA. DTI is based on the diffusion
of water molecules. Water tends to move faster
along nerve fibers rather than perpendicular to
them. In healthy individuals, white matter diffusion
is more organized in a specific direction; this is
known as anisotropy. FA is believed to reflect many
factors, including the degree of myelination and
axonal density/integrity. FA Values range from 0 to 1, where 0 represents isotropic diffusion or lack of
directional organization and 1 represents anisotropic
diffusion or diffusion restricted to one direction. In
most studies FA is decreased in patients with mTBI
and TBI.50 The technology is a modification of diffusion
weighted imaging and determines white matter
integrity and is sensitive to changes in white matter
microstructure. It's also specific to each individual
scanner and therefore prior to institution, each imaging
center must develop their own set of normal values
and specific DTI protocol, which the operator
and radiologist will then use to manually outline the
specific regions of interest.50 Most imaging centers
use region of interest analysis (ROI) where white
matter FA is measured in specific regions of the
brain. The measured FA is then compared to a database
of normal patients. ROI is useful for testing
hypotheses regarding the relation of white matter
integrity in a specific neuro-anatomical region to an
outcome variable, and a 1.5 to 2 standard deviation
in the FA is considered abnormal.50

A majority of the studies using DTI have been in
patients with mTBI and TBI. The Kraus paper, published
in Brain in 2007,51 is considered the landmark
paper for DTI methodology with respect to TBI.
Region of interest analysis included the anterior and
posterior corona radiata, corticospinal tracts, cingulum,
external capsule, forceps major and minor,
genu, corpus callosum, inferior fasciculus, superior
longitudinal fasciculus. The primary objective was to
characterize white matter integrity utilizing DTI
across the spectrum of chronic TBI of all severities.
Secondary objectives included examining the relationship
between white matter integrity and cognition.
The researchers looked at 20 mild and 17 moderate/
severe TBI patients and 20 controls who
underwent DTI and neuropsychological testing with
FA being the primary measure of white matter
integrity. Moderate to severe TBI patients showed
decreased white matter FA in all ROI. Mild TBI
patients showed decreased FA in the corticospinal
tracts, sagittal stratum and superior longitudinal fasciculus.
Cubon, et al. 201152 assessed WM fiber tract
integrity using tract-based spatial statistics (TBSS) in
10 varsity college athletes and controls. They also
included moderate and severe TBI patients and controls.
Athletes still symptomatic one month after
sports-related concussion demonstrated increased
mean diffusivity (MD) in several WM tracts in the
left hemisphere including the inferior and superior
longitudinal fasciculus, fronto-occipital fasciculi,
retrolenticular part of internal capsule, posterior
thalamic and acoustic radiations. There was no difference
in fractional anistropy (FA) between athletes
and controls, however FA decreased with the level of
severity. This could be interpreted that the athletes
FA's were abnormal as the study's controls actually
had moderate to severe TBI. The researchers concluded
that FA may be more sensitive in detecting
severe injury and MD may be more sensitive in
detecting mild injury. In a similar study Henry et al
201153 investigated the effects of sports concussion
on white matter integrity using three different
Diffusion Tensor Imaging measures (FA, axial diffusion
AD, and MD) by comparing a group of 10 nonconcussed
athletes with a group of 18 concussed
athletes of the same age (mean: 22.5 years) and education
(mean: 16 years) using a voxel-based approach
(VBA) within both the acute and chronic post-injury
phases, i.e. at one to six days post-concussion and
again six months later. FA was increased in dorsal
regions of both cortical spinal tracts (CST) and in the
corpus callosum in concussed athletes at both time
points. AD at both time points was elevated in the
right cortical spinal tracts. MD values were
decreased in concussed athletes in the cortical spinal
tracts (CST) and corpus callosum at both time
points. Although there was some limitation in the
technique used to image large fiber tracts, the
authors concluded that sports concussions result in
changes in diffusivity in the corpus callosum and
CST of concussed athletes.

Conclusion

There are a number of tools to assist the physician
in assessing and returning an athlete to play.
Computerized and formal, i.e. paper and pencil,
neuropsychological testing have been the most widely
studied and validated. Neuroimaging studies especially
DTI MRI hold significant promise as an objective measure for the future. However none of the
testing is completely objective and therefore should
never be used alone when evaluating and considering
returning an athlete to play.

AAN Sports Neurology Position Statement

Any athlete suspected of suffering a concussion should be
removed from participation until evaluated by a physician.

No athlete should be allowed to participate in sports if they are
still experiencing symptoms of a concussion.

Following a concussion a physician, preferably a neurologist,
should be consulted prior to clearing the athlete to return to
participation.

A certified coach or athletic trainer should be present at all
sporting events, including practices, where risk of concussion is
involved.

Education efforts should be maximized to improve the understanding
of concussion by all athletes, parents, and coaches.

An athlete must be completely asymptomatic (cognitively/
physically), off of any concussion related medications) and complete
a graded protocol prior to RTP.

Note: This is an updated version of the original released in 2010.
Point #6 has since been added.

Part III of this series will appear in the
January/February edition. Part I appeared in
September/October. Visit PracticalNeurology.net to
download the entire three-part article.

Dr. Conidi is the Director of the Florida Center for
Headache and Sports Neurology, the team Neurologist
for the NHL's Florida Panthers and is an Assistant
Clinical Professor of Neurology at Florida State
University College of Medicine. He has been elected to
serve on the American Academy of Neurology's Sports
Neurology Executive Committee and is a consultant for
the FDA's Center for Devices and Radiological Health
(CDRH), which deals specifically with sports concussion.
Please direct any questions and comments to
fxneuro@bellsouth.net.

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